Neural correlates of fixation duration in natural reading: Evidence from fixation-related fMRI

A key assumption of current theories of natural reading is that fixation duration reflects underlying attentional, language, and cognitive processes associated with text comprehension. The neurocognitive correlates of this relationship are currently unknown. To investigate this relationship, we compared neural activation associated with fixation duration in passage reading and a pseudo-reading control condition. The results showed that fixation duration was associated with activation in oculomotor and language areas during text reading. Fixation duration during pseudo-reading, on the other hand, showed greater involvement of frontal control regions, suggesting flexibility and task dependency of the eye movement network. Consistent with current models, these results provide support for the hypothesis that fixation duration in reading reflects attentional engagement and language processing. The results also demonstrate that fixation-related fMRI provides a method for investigating the neurocognitive bases of natural reading.

[1]  C. Price,et al.  Phonological decisions require both the left and right supramarginal gyri , 2010, Proceedings of the National Academy of Sciences.

[2]  John M. Henderson,et al.  Oculomotor Inhibition of Return in Normal and Mindless Reading , 2012 .

[3]  René M. Müri,et al.  The parietal cortex and saccade planning: lessons from human lesion studies , 2013, Front. Hum. Neurosci..

[4]  K. Rayner,et al.  Mindless reading revisited: Eye movements during reading and scanning are different , 1996, Perception & psychophysics.

[5]  S. Liversedge,et al.  Oxford handbook of eye movements , 2011 .

[6]  Steven G. Luke,et al.  Stable individual differences in saccadic eye movements during reading, pseudoreading, scene viewing, and scene search. , 2014, Journal of experimental psychology. Human perception and performance.

[7]  J. Henderson,et al.  Using CRISP to model global characteristics of fixation durations in scene viewing and reading with a common mechanism , 2012 .

[8]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[9]  R. Wurtz,et al.  Organization of monkey superior colliculus: enhanced visual response of superficial layer cells. , 1976, Journal of neurophysiology.

[10]  Jeffrey D. Schall.  Frontal Eye Fields , 2009 .

[11]  Michael S. Beauchamp,et al.  A new method for improving functional-to-structural MRI alignment using local Pearson correlation , 2009, NeuroImage.

[12]  Michael C. Dorris,et al.  The role of posterior parietal cortex in the regulation of saccadic eye movements , 2011 .

[13]  William W. Graves,et al.  Neural Systems for Reading Aloud: A Multiparametric Approach , 2009, Cerebral cortex.

[14]  M. Kronbichler,et al.  Fixation-Related fMRI Analysis in the Domain of Reading Research: Using Self-Paced Eye Movements as Markers for Hemodynamic Brain Responses During Visual Letter String Processing , 2013, Cerebral cortex.

[15]  William W. Graves,et al.  Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. , 2009, Cerebral cortex.

[16]  John M. Henderson,et al.  Morphology of Primary Visual Cortex Predicts Individual Differences in Fixation Duration during Text Reading , 2014, Journal of Cognitive Neuroscience.

[17]  J. B. Preston,et al.  Interconnections between the prefrontal cortex and the premotor areas in the frontal lobe , 1994, The Journal of comparative neurology.

[18]  C. Price.  The anatomy of language: a review of 100 fMRI studies published in 2009 , 2010, Annals of the New York Academy of Sciences.

[19]  Jun Tanji,et al.  Prefrontal cortical cells projecting to the supplementary eye field and presupplementary motor area in the monkey , 2005, Neuroscience Research.

[20]  Robin K. Morris,et al.  Phonological codes are used in integrating information across saccades in word identification and reading. , 1992, Journal of experimental psychology. Human perception and performance.

[21]  Steven G. Luke,et al.  Co-registration of eye movements and event-related potentials in connected-text paragraph reading , 2013, Front. Syst. Neurosci..

[22]  Joseph T. Devlin,et al.  Supramarginal gyrus involvement in visual word recognition , 2009, Cortex.

[23]  R. Wurtz,et al.  Role of the rostral superior colliculus in active visual fixation and execution of express saccades. , 1992, Journal of neurophysiology.

[24]  S. Heim,et al.  Identifying brain systems for gaze orienting during reading: fMRI investigation of the Landolt paradigm , 2013, Front. Hum. Neurosci..

[25]  J. Henderson,et al.  Neural correlates of active vision: An fMRI comparison of natural reading and scene viewing , 2015, Neuropsychologia.

[26]  Eyal M. Reingold,et al.  Neurophysiological constraints on the eye-mind link , 2013, Front. Hum. Neurosci..

[27]  J. Henderson,et al.  Effects of foveal processing difficulty on the perceptual span in reading: Implications for attention and eye movement control. , 1990 .

[28]  Cathy J. Price,et al.  A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading , 2012, NeuroImage.

[29]  Philipp Koehn,et al.  Cognitive Psychology , 1992, Ageing and Society.

[30]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[31]  G. E. Smith.  The Human Brain , 1924, Nature.

[32]  C. Pierrot-Deseilligny,et al.  Eye movement control by the cerebral cortex , 2004, Current opinion in neurology.

[33]  Reinhold Kliegl,et al.  SWIFT: a dynamical model of saccade generation during reading. , 2005, Psychological review.

[34]  J. O'Regan,et al.  Mindless reading: Eye-movement characteristics are similar in scanning letter strings and reading texts , 1995, Perception & psychophysics.

[35]  René M. Müri,et al.  Neurophysiology and neuroanatomy of reflexive and volitional saccades as revealed by lesion studies with neurological patients and transcranial magnetic stimulation (TMS) , 2008, Brain and Cognition.

[36]  Erik D. Reichle,et al.  Toward a model of eye movement control in reading. , 1998, Psychological review.

[37]  Erik D. Reichle,et al.  Serial-attention models of reading , 2011 .

[38]  John M. Henderson,et al.  Temporal oculomotor inhibition of return and spatial facilitation of return in a visual encoding task , 2013, Front. Psychol..

[39]  Bernard Mazoyer,et al.  Meta-analyzing left hemisphere language areas: Phonology, semantics, and sentence processing , 2006, NeuroImage.

[40]  A. Owen,et al.  Anterior prefrontal cortex: insights into function from anatomy and neuroimaging , 2004, Nature Reviews Neuroscience.

[41]  John M. Henderson,et al.  Neural Correlates of Fixation Duration during Real-world Scene Viewing: Evidence from Fixation-related (FIRE) fMRI , 2015, Journal of Cognitive Neuroscience.

[42]  C. Clifton,et al.  Stress Matters: Effects of Anticipated Lexical Stress on Silent Reading. , 2011, Journal of memory and language.

[43]  Rutvik H. Desai,et al.  The neural substrates of natural reading: a comparison of normal and nonword text using eyetracking and fMRI , 2014, Front. Hum. Neurosci..

[44]  Guinevere F. Eden,et al.  Meta-Analysis of the Functional Neuroanatomy of Single-Word Reading: Method and Validation , 2002, NeuroImage.

[45]  Stefan Everling,et al.  Frontal cortex and flexible control of saccades , 2011 .

[46]  John M. Henderson,et al.  EVIDENCE FOR THE USE OF PHONOLOGICAL REPRESENTATIONS DURING TRANSSACCADIC WORD RECOGNITION , 1995 .

[47]  Stephen M. Rao,et al.  Human Brain Language Areas Identified by Functional Magnetic Resonance Imaging , 1997, The Journal of Neuroscience.

[48]  C. Kennard,et al.  Functional role of the supplementary and pre-supplementary motor areas , 2008, Nature Reviews Neuroscience.

[49]  R. E. Morrison,et al.  Manipulation of stimulus onset delay in reading: evidence for parallel programming of saccades. , 1984, Journal of experimental psychology. Human perception and performance.

[50]  Erik D. Reichle,et al.  The E-Z Reader model of eye-movement control in reading: Comparisons to other models , 2003, Behavioral and Brain Sciences.

[51]  K. Rayner.  The 35th Sir Frederick Bartlett Lecture: Eye movements and attention in reading, scene perception, and visual search , 2009, Quarterly journal of experimental psychology.

[52]  K. Rayner.  Eye movements in reading and information processing: 20 years of research. , 1998, Psychological bulletin.

[53]  A. Friederici.  The cortical language circuit: from auditory perception to sentence comprehension , 2012, Trends in Cognitive Sciences.

[54]  Frans W Cornelissen,et al.  Fixation based event‐related fmri analysis: Using eye fixations as events in functional magnetic resonance imaging to reveal cortical processing during the free exploration of visual images , 2012, Human Brain Mapping.

[55]  J. Henderson,et al.  Effects of foveal processing difficulty on the perceptual span in reading: implications for attention and eye movement control. , 1990, Journal of experimental psychology. Learning, memory, and cognition.

[56]  David C. Van Essen,et al.  Application of Information Technology: An Integrated Software Suite for Surface-based Analyses of Cerebral Cortex , 2001, J. Am. Medical Informatics Assoc..

[57]  John M. Henderson,et al.  Oculomotor and cognitive control of eye movements in reading: Evidence from mindless reading , 2013, Attention, Perception, & Psychophysics.

[58]  G. Rizzolatti,et al.  Corticocortical connections of area F3 (SMA‐proper) and area F6 (pre‐SMA) in the macaque monkey , 1993, The Journal of comparative neurology.

[59]  J. Henderson,et al.  Oculomotor inhibition of return in normal and mindless reading , 2012, Psychonomic bulletin & review.

[60]  J. D. Connolly,et al.  fMRI activation in the human frontal eye field is correlated with saccadic reaction time. , 2005, Journal of neurophysiology.

[61]  T. Paus,et al.  Cortical regions involved in eye movements, shifts of attention, and gaze perception , 2005, Human brain mapping.

[62]  Jeffrey R. Binder,et al.  Where is the Semantic System ? , 2009 .

[63]  M. Torrens.  Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[64]  E. Koechlin,et al.  Anterior Prefrontal Function and the Limits of Human Decision-Making , 2007, Science.

[65]  Ralf Engbert,et al.  Mindless reading revisited: An analysis based on the SWIFT model of eye-movement control , 2009, Vision Research.